Fomite Transmission Follows Invasion Ecology Principles

ABSTRACT The invasion ecology principles illustrated in many ecosystems have not yet been explored in the context of fomite transmission. We hypothesized that invaders in fomite transmission are trackable, are neutrally distributed between hands and environmental surfaces, and exhibit a proximity effect. To test this hypothesis, a surrogate invader, Lactobacillus delbrueckii subsp. bulgaricus, was spread by a root carrier in an office housing more than 20 participants undertaking normal activities, and the microbiotas on skin and environmental surfaces were analyzed before and after invasion. First, we found that the invader was trackable. Its identity and emission source could be determined using microbial-interaction networks, and the root carrier could be identified using a rank analysis. Without prior information, L. bulgaricus could be identified as the invader emitted from a source that exclusively contained the invader, and the probable root carrier could be located. In addition to the single-taxon invasion by L. bulgaricus, multiple-taxon invasion was observed, as genera from sputum/saliva exhibited co-occurrence relationships on skin and environmental surfaces. Second, the invader had a below-neutral distribution in a neutral community model, suggesting that hands accrued heavier invader contamination than environmental surfaces. Third, a proximity effect was observed on a surface touch network. Invader contamination on surfaces decreased with increasing geodesic distance from the hands of the carrier, indicating that the carrier’s touching behaviors were the main driver of fomite transmission. Taken together, these results demonstrate the invasion ecology principles in fomite transmission and provide a general basis for the management of ecological fomite transmission. IMPORTANCE Fomite transmission contributes to the spread of many infectious diseases. However, pathogens in fomite transmission typically are either investigated individually without considering the context of native microbiotas or investigated in a nondiscriminatory way from the dispersal of microbiotas. In this study, we adopted an invasion ecology framework in which we considered pathogens as invaders, the surface environment as an ecosystem, and human behaviors as the driver of microbial dispersal. With this approach, we assessed the ability of quantitative ecological theories to track and forecast pathogen movements in fomite transmission. By uncovering the relationships between the invader and native microbiotas and between human behaviors and invader/microbiota dispersal, we demonstrated that fomite transmission follows idiosyncratic invasion ecology principles. Our findings suggest that attempts to manage fomite transmission for public health purposes should focus on the microbial communities and anthropogenic factors involved, in addition to the pathogens.


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Wang et al. present an interesting experiment on the transmission of an introduced bacterial contaminant through an office environment with context to the native host and surface microbiota. The main results are in line with expectations; e.g., (i) participant hands became the most frequently "contaminated" site sampled (probably because they have the highest degree of touch network relative to other sites sampled) and (ii) proximity effect of source of transmission. While the experimental design is sound, and this could be a nice benchmarking study for sitespecific bacterial transmission, the broader invasion ecology applications and explanations for findings seem speculative. Some re-direction may help improve the manuscript prior to publication. Comments below.
1. The implication of invasion ecology driving the observed microbiota transitions seems like a reach for the scope of the experiment. Continuous introduction of the contaminant bacterial strain every 30 mins, along with the network of surface touching (stemming outward from the carrier) are probably the primary drivers of contaminant transmission. As such, the flux in relative abundances of host/surface microbiota observed between the two time points (morning and end of day) are probably just related to the physical introduction of L. bulgaricus, mainly at high-touch surfaces. I am not sure it is "invading" as much as it is physically tracking across space and time. There is discussion about ecology and evolution in the text, though L. bulgaricus is most likely passively dispersed and not growing in the environments being sampled (or at least was not measured to be). Do the data show otherwise? 2. I think the focus of the paper would be stronger if re-framed as a benchmarking experiment to model fomite transmission using 16S amplicon abundances to get at questions like: How accurately can we model transmission with these data, and what are parameters for proximity effects in this specific space? What is the variation across the experimental systems? How does this relate to other fomite transmission models (I am not an epidemiologist by the way, so am personally not sure)? 3. The authors' previous report is similar: https://www.sciencedirect.com/science/article/pii/S0304389421011018#fig0005. Fig. S1 looks nearly identical to the Fig. 1 from that report, with the key difference being quantification method of L. bulgaricus (i.e., amplicon relative abundance here vs. single-gene qPCR copy number there). Please expand on key differences to validate novelty in publishing the current study. 4. The results and figures present contaminant transmission as measured relative abundances among microbiota, sometimes among relative abundances of genera, species, and ASVs. Why are different taxonomic levels used throughout the paper as means for the quantification? Resolution should probably not go finer than species, considering multiple ASVs map to L. bulgaricus (which may even suggest potential problems for tracking it as a model strain). Please be consistent or explain. 5. The introduction and discussion provide considerable focus on phenomena that may lack relevance to the specific context of the study. Pulmonary/sputum/oral/gut microbiomes are mentioned, even as sources to the observed environmental sample, but they were not sampled here. To my knowledge, built environment surface microbiomes look mostly like a mix of environmental and skin-derived microbiota, and that is probably what is seen here as well. 6. Please expand on limitations in the discussion. 7. Thank you for making the sequencing data public. Your manuscript has been accepted, and I am forwarding it to the ASM Journals Department for publication. For your reference, ASM Journals' address is given below. Before it can be scheduled for publication, your manuscript will be checked by the mSystems production staff to make sure that all elements meet the technical requirements for publication. They will contact you if anything needs to be revised before copyediting and production can begin. Otherwise, you will be notified when your proofs are ready to be viewed.
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